Estuarine Production of Resident and Nursery Fish Species

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Estuarine, Coastal and Shelf Science 78 (2008) 51e60 www.elsevier.com/locate/ecss

Estuarine production of resident and nursery ﬁsh species: Conditioning by drought events?

M. Dolbeth a,*, F. Martinho a, I. Viegas a, H. Cabral b, M.A. Pardal a

a Institute of Marine Research (IMAR), c/o Department of Zoology, University of Coimbra, 3004-517 Coimbra, Portugal b Instituto de Oceanograﬁa, Faculdade de Cieˆncias da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal Received 3 August 2007; accepted 19 November 2007 Available online 8 December 2007

Abstract

The production of resident (Pomatoschistus minutus and Pomatoschistus microps) and marine juvenile fish species using the Mondego estuary (central Portugal) as nursery grounds (Dicentrarchus labrax, Platichthys flesus, Solea solea), was assessed in order to: (1) understand the potential of the estuary for fish production; (2) know the production of nursery fish species likely to be exported to the coastal stocks; and (3) how anthropogenic and natural stress could influence the estimated production. Sampling occurred from June 2003 to May 2006 and together the 5 species in study comprised around 70% of the whole fish community numbers and biomass. Increasing drought conditions were observed, starting with a normal hydrological year in 2003 until attaining a severe drought in 2005, which resulted in low river discharges (1/3 of the mean river discharges in 2003). Additionally, high water temperatures were observed in 2003 and 2005 (24 and 26 C, night temperatures). The secondary production was estimated using the increment summation method, after recognition of the cohorts. Production was in general lower in the Mondego estuary when compared to other systems, which was associated to the estuary’s small area (only 3.4 km2, less than 1/4 of area compared to other studied systems). Dicentrarchus labrax was among the most productive species. Production decreased in the drought year for all species, especially evident for D. labrax, P. minutus and P. flesus. No direct effects could be attributable to the salinity and temperature variations and to the low freshwater discharges (resulting from the drought and high temperatures), yet these were pointed as probable major reasons for the decreased production. A significant reduction (15e45% reduction in the estuarine production) was also concluded for the potential production to be exported for coastal areas by the nursery species in the drought conditions. Ó 2007 Elsevier Ltd. All rights reserved.

Keywords: ﬁsh production; resident species; nursery species; drought; Mondego estuary

1. Introduction Martinho et al., 2007b). The juvenile growth and survival of the marine species, hence recruitment into adult populations, Estuarine systems are extremely valuable for many marine and the maintenance of the resident species within the estua- fish species of the continental shelf, by providing important rine ecosystem are greatly determined by its environmental nursery grounds (Cabral et al., 2007; Martinho et al., 2007a; quality, regarding both anthropogenic stress and natural Nicolas et al., 2007), as well as for several other fishes, such variability (Nicolas et al., 2007). The availability of essential as the resident ones, spending their complete life cycle within habitats (such as seagrasses and saltmarshes), providing pro- the estuary (Elliott and Dewailly, 1995; Dolbeth et al., 2007a). tection from predators, and their great production, providing Frequently, these two ecological fish guilds (marine juvenile abundant food supplies, are considered as major determinants and resident) represent the major part of the fish community for fishes in estuaries (Beck et al., 2001; Cabral et al., 2007; found in estuarine systems (Elliott and Dewailly, 1995; Martinho et al., 2007a). Several of the marine juvenile fishes that occur in estuaries are commercially important, hence * Corresponding author. estuaries may be considered as essential ecosystems for the E-mail address: [email protected] (M. Dolbeth). renewal of fisheries resources, acquiring also a direct relevant

FIGUEIRA DA FOZ economic value for mankind (Houde and Rutherford, 1993; 8°50’W M Cowley and Whitﬁeld, 2002; Able, 2005; Nicolas et al., NORTH ARM 2007). Regarding resident species, their role as intermediates N1 1Km in the estuarine food web turns them crucial for the overall dy- N2 40°08’N namics and functioning of the estuarine system (Leit~ao et al., SOUTH ARM

2006; Dolbeth et al., 2007a). Yet, estuarine areas are highly af- ATLANTIC OCEAN fected by human activities such as habitat reclamation, water

DEGO RIVER quality impoverishment and fishing activities (Cabral et al., S1 2007; Vasconcelos et al., 2007) and are known for their high MON natural environmental variability (Maes et al., 2004; Elliott PRANTO S2 and Quintino, 2007). In this perspective, understanding the RIVER potential of estuarine areas for these fishes production and INTERTIDAL AREAS SLUICE SAMPLING the influence of external environmental or anthropogenic im- PORTUGAL SALTMARSHES STATIONS pacts on that production becomes quite relevant. This information may be useful as a tool to support protection measures and Fig. 1. The Mondego estuary, with indication of the sampling stations, inter- ensure resource sustainability, or for the study of the overall tidal area and saltmarshes. estuarine ecological integrity. In fact, production estimates in- tegrate the influence of numerous biotic variables and environmental conditions affecting individual growth and population from the Pranto river (Fig. 1), as the upstream areas are almost mortality (Cusson and Bourget, 2005; Dolbeth et al., 2005). silted up, with only a small connection with north arm. The Therefore, production studies have been used to assess the im- Pranto river is controlled by a sluice according to the water pacts of natural and anthropogenic stressors (Cardoso et al., needs in the rice fields of Mondego valley. The downstream 2005; Dolbeth et al., 2005, 2007b), in ecosystem modelling areas of the south arm are relatively unchanged, with Spartina studies (energy budgets and flows, Gamito and Erzini, 2005; maritima marshes and a Zostera noltii meadow, but in the in- Patrıćio and Marques, 2006), and for fish assemblages have ner parts the seagrass community has completely disappeared, been used more frequently to assess the potential yields for mainly due to severe eutrophication problems occurring in the fishery species (Houde and Rutherford, 1993; Wilson, 2002; past (Lillebø et al., 2005; Dolbeth et al., 2007b). In 1998/1999 Pombo et al., 2007). mitigation measures were taken to reduce the nutrient loading The present study aims to estimate the secondary produc- and the system seems to be gradually recovering (for further tion of the resident and marine juvenile fish species of the details see Cardoso et al., 2005; Dolbeth et al., 2007b). Mondego estuary (central Portugal). More specifically, it aims to understand: (1) the productive potential of the estuary 2.2. Sampling procedures for the fish resources, and ultimately for other consumers; (2) the production potential to be exported by the marine juveniles From June 2003 to May 2006 fish were collected monthly, to the coastal stocks (infer on the production produced in the using a 2 m beam trawl, with one tickler chain and 5 mm estuary transferred to the coastal areas); and (3) how anthropo- stretched mesh size in the cod end. Sampling was carried genic and natural stress influence the production estimates. out during the night, at the ebbing tide of spring tides, at five stations (M, S1, S2, N1, N2, Fig. 1): M e at 1.5 km 2. Material and methods from the estuary’s mouth, 8.7 1.2 m deep, area subjected to constant dredging; S1 e located upstream a Zostera noltii 2.1. Study site bed, 2.3 0.4 m deep; S2 e near the Pranto river sluices, which controls the main freshwater flow from Pranto river to The Mondego estuary (Portugal) is located in a warm tem- the south arm, 2.4 1.0 m deep; N1 e with regular freshwater perate region, on the Atlantic coast of Portugal (40080N, flow, 5.5 0.5 m deep; N2 e most upstream area, with lower 8500W) (Fig. 1). It is a small estuary (3.4 km2 area), with saline influence and permanent freshwater flow from the two arms (north and south) of distinct hydrologic characteris- Mondego river, 4.5 0.3 m deep. Each survey consisted of tics. The north arm is deeper (4e10 m during high tide, tidal three hauls, at each sampling station, in a total of 10e range 1e3 m), it is a main navigation channel and is the loca- 15 min duration per station. All fish caught were identified, tion of the Figueira da Foz harbour. Besides the severe measured (total length, with 1 mm precision) and weighted changes imposed by the construction of harbour facilities, (wet weight e WW, with 0.001 g precision). A detailed de- constant dredging and shipping occurs in this area, causing scription of the community structure is provided in Martinho physical disturbance of the bottom. The main freshwater input et al. (2007b). Due to the amount of data required for the pro- to the north arm is from the Mondego river. The south arm is duction estimates, only the most abundant fish species, along shallower (2e4 m during high tide, tidal range 1e3 m), char- the surveyed period, were used in the present study, i.e. the acterized by large areas of exposed intertidal flats during low marine juveniles using the estuary as nursery grounds e nurs- tide (about 75% of total area). Water circulation in the south ery species, Dicentrarchus labrax, Platichthys flesus, Solea arm mostly depends on the tides and on the freshwater input solea and the residents Pomatoschistus minutus and M. Dolbeth et al. / Estuarine, Coastal and Shelf Science 78 (2008) 51e60 53

Pomatoschistus microps, which live in the estuary throughout 3. Results their life cycle (nursery and resident ecological guilds, adapted from Elliott and Dewailly, 1995, and according to Martinho 3.1. Environmental background et al., 2007b). In each sampling station, water transparency and depth From June 2003 to May 2006, precipitation showed were registered, and dissolved oxygen, temperature, pH and unusual variations when compared to the mean precipitation salinity were measured from the water collected near the bot- regime for central Portugal observed during the period of tom. Precipitation values were acquired in the Casal do Rato 1940e1997 (annual precipitation values of 1030 mm, INAG e 13D/04UG station, from INAG e Portuguese Water Institute http://snirh.inag.pt)(Fig. 2A). All years had lower annual pre- (available in http://www.snirh.inag.pt). Freshwater runoff cipitation values when compared to the 1940e1997 mean, es- was acquired from INAG station Açude Ponte Coimbra 12G/ pecially in 2004 and 2005, considered as dry years. The lowest 01A, near the city of Coimbra (located 40 km upstream). annual precipitation was observed in 2005 (486.1 mm), with below-mean precipitation periods quite evident practically 2.3. Secondary production during all year (from January until September 2005) e extreme drought (Fig. 2A). The freshwater runoff from the The population structure of each species was defined by Mondego river basin had a severe reduction in 2005, with tracking recognizable cohorts from the successive sampling dates. Spatial samples were pooled together and analyzed through size frequency distribution of successive sampling A Precipitation and water runoff dates. For Dicentrarchus labrax, Platichthys flesus and Solea 300 6000 Wtater runoff (10 solea the cohorts were determined using FAOICLARM Stock 250 5000 Assessment Tools (FiSAT software, provided in http://www. 200 4000 fao.org/fi/statist/fisoft/fisat/index.htm). For Pomatoschistus 150 3000 minutus and Pomatoschistus microps, as the class interval for the length frequency analyses was lower than 0.25 cm, 100 2000 5

50 1000 m

ANAMOD software package was used, which provided the Precipitation (mm) 3 modes and their standard deviation, and checked the reliability 0 0 )

of the estimated parameters. This analysis is described in J-03 J-03 J-04 J-04 J-04 J-05 J-05 J-05 F-04 F-06 A-03 S-03 A-04 A-04 S-04 A-05 A-05 S-05 A-06 A-06 N-03 D-03 N-04 D-04 N-05 D-05 O-03 O-04 O-05 M-04 M-04 M-05 M-05 M-05 M-06 M-06 Dolbeth et al. (2007a). Precipitation (1940-1997) Precipitation Water runoff After recognition of the cohorts, the annual production was estimated by the cohort increment summation method B Mean water temperature (Winberg, 1971), according to: 30 XT1 25 Nt þ Ntþ1 Pcn ¼ ðwtþ1 wtÞ 20 t¼0 2 ºC 15 2 1 where Pcn is the growth production (g WW m y ) of cohort 10 n; N is the density (ind m2); w is the mean individual weight (g WW m2); and t and t þ 1, consecutive sampling dates. 5 J-03 J-03 J-04 J-04 J-04 J-05 J-05 J-05 J-06 F-04 F-05 F-06 A-04 A-05 A-06 A-03 S-03 A-04 S-04 A-05 S-05 N-03 D-03 N-04 D-04 N-05 D-05

Population production estimates correspond to the sum of O-03 O-04 O-05 M-04 M-04 M-05 M-05 M-06 M-06 each cohort production (Pcn). Negative production values were not accounted for the overall fish estimates, which C Salinity were regarded as no production. Production estimates were 40 35 also presented with the correction for the catch efficiency of 30 the sampling gear (beam trawl), which according to 25 Hemingway and Elliott (2002) is 30%. 20 The mean annual biomass (B) was estimated according to: 15 10 1 XNc 5 B ¼ ðBcntcnÞ 0 T n¼1 J-04 J-04 J-05 J-05 J-05 J-06 J-03 J-03 J-04 F-05 F-06 F-04 A-04 S-04 A-05 S-05 A-03 S-03 A-04 A-05 A-06 N-04 D-04 N-03 D-03 N-05 D-05 O-04 O-05 O-03 M-04 M-04 M-05 M-05 M-06 M-06 where T is the period of study, which is always 365 days M S1 S2 N1 N2 (yearly cycles) as the mean annual biomass is being computed; Fig. 2. Temporal variations of: (A) precipitation during the study period and Nc is the number of cohorts found in the study period; Bcn is 2 mean precipitation for central Portugal during the period of 1940e1997 and the mean biomass (g WW m ) of cohort n; tcn is the time freshwater runoff to the Mondego estuary; (B) mean estuarine water temper- period of the cohort n (days), from the first appearance of ature standard deviation for the whole Mondego estuary; and (C) salinity individuals until they disappeared. in the different sampling stations of the Mondego estuary. 54 M. Dolbeth et al. / Estuarine, Coastal and Shelf Science 78 (2008) 51e60 values considerably lower (on average 1/3 lower, until Octo- study period for the fish species in study, with the highest ber the water runoff was always lower than 350 105 m3) values observed in 2003/04, almost two-fold the values occur- than the ones observed in 2003 and 2006 (Fig. 2A). Conse- ring in 2005/06 (Table 1). For each species alone, this ten- quently, salinity was highly variable, with the highest values dency was maintained for the mean density values, yet both observed in 2005 (Fig. 2B). Spatially, in the estuary’s mouth Platichthys flesus and Solea solea had higher production values (station M) salinity presented typical values for marine water, in 2004/05 than in the other years (Table 1). Pomatoschistus except for the winter 2006 (Fig. 2B). In general, higher salin- microps maintained similar values of mean biomass and pro- ities were recorded in the south arm (stations S1 and S2) than duction throughout the three-year study period (Table 1). in the north arm (N1 and N2) (Fig. 2B). Station S1 showed Comparing all species, the highest production values, highest similar values to the ones recorded in the estuary’s mouth mean density and biomass were observed for Dicentrarchus (M), while stations S2 and N1 presented typical brackish wa- labrax (except for the mean biomass in 2005/06). Solea solea ter values (Fig. 2B). The most upstream area (station N2) was the second most productive species, with the highest showed the lowest salinities, ranging between 0 and 2 production obtained in 2004/05 (Table 1). The resident (Fig. 2B). Yet, in 2005, abnormal high salinities were species Pomatoschistus minutus and P. microps had the lowest observed (14.0 6.46 from February 05 to September 05, mean biomass values and the lowest production estimates Fig. 2B), due to low precipitation and low freshwater runoff (Table 1). In fact, P. microps was the least productive species, (extreme drought, Fig. 2A). although it attained high densities (Table 1). The P/ B ratios Water temperature showed variations usually found in temper- ranged from 1.3 (for P. minutus) to 3.9 (for S. solea), with ate systems, with increasing values in the spring (MarcheJune), no clear tendency variation (Table 1). Pomatoschistus microps until reaching the highest values in the summer (JulyeSeptem- was the only species that maintained similar P/ B ratios ber) and lowest values in the winter periods (DecembereFebru- through the three-year study period (Table 1). ary). In July 2003 and July 2005 higher temperatures were The trend of the annual density, biomass and production observed when compared to the same period in 2004, with the values was clarified with the study of their tendencies along highest values recorded in the upstream sampling stations the three-year study period (Figs. 3 and 4). The highest pro- (24 Ce26 C night temperature at S2 and N2) (Fig. 2B). duction peaks were observed for Dicentrarchus labrax in More information on the environmental and hydrological 2003 (Fig. 4A), together the highest increase in density parameters (e.g. dissolved oxygen, pH, water transparency, (Fig. 3A). By the end of 2004 and beginning of 2005 it was chlorophyll a) is reported in Dolbeth et al. (2007a) and observed another peak in production (Fig. 4A), but now asso- Marques et al. (2007). ciated an increase in biomass (Fig. 3A). During the period of 2005/06, density, biomass and production were lower (Figs. 3.2. Fish density, biomass and production 3A and 4A). For Solea solea the highest peaks in production were observed by the end of 2004 and in 2005 (Fig. 4B) to- Mean annual density, biomass and production of the com- gether with the high increases of density and biomass munity estimates showed a clear decreasing trend along the (Fig. 3B). Density was highest in the beginning of 2003, yet

Table 1 Annual mean density (Ind m2), mean biomass (g WW m2), production (g WW m2 y1) and P/ B ratios for each species and the fish community in study. Between brackets production values after correction for the catch efficiency of the beam trawl (30%) D. labrax S. solea P. flesus P. minutus P. microps All Density (Ind m2) 2003/04 0.0150 0.0024 0.0025 0.0076 0.0088 0.036 2004/05 0.0031 0.0012 0.0017 0.0011 0.0083 0.015 2005/06 0.0029 0.0013 0.0005 0.0017 0.0046 0.011 Biomass (g WW m2) 2003/04 0.10 0.07 0.05 0.005 0.0013 0.22 2004/05 0.08 0.06 0.05 0.002 0.0013 0.19 2005/06 0.04 0.09 0.02 0.001 0.0010 0.15 Production (g WW m2 y1) 2003/04 0.44 0.19 0.11 0.017 0.0036 0.77 (1.47) (0.65) (0.38) (0.056) (0.012) (2.57) 2004/05 0.20 0.24 0.13 0.004 0.0030 0.57 (0.67) (0.78) (0.42) (0.012) (0.011) (1.91) 2005/06 0.14 0.19 0.07 0.002 0.0030 0.39 (0.48) (0.63) (0.22) (0.005) (0.010) (1.31) P/ B(y1) 2003/04 4.3 3.0 2.3 3.3 2.7 3.5 2004/05 2.5 3.9 2.8 2.1 2.4 3.1 2005/06 3.2 2.1 3.6 1.3 2.9 2.6 M. Dolbeth et al. / Estuarine, Coastal and Shelf Science 78 (2008) 51e60 55

A 0.09 D. labrax A 500 35 -1

) D. labrax 450 Density (Ind m -2 30 400 0.06

350 25 month

300 20 -2 250 0.03 200 15 150 10 g WW m 100 -2 0 5 ) J J J J J J J J F F F S S S A A A A A A N D N D N D O O O M M M M 50 M M Biomass (g WW m 0 0 J J J J J J J J J F F F S S S A A A A A A N D N D N D O O O M M M M M M B 0.09 S. solea -1 B 450 8

) S. solea 0.06

400 Density (Ind m -2 7 350 month

6 -2 300 5 0.03 250 4 200

3 g WW m 150 0 J J J J J J J J F F F S S S A A A A 2 A A -2 N D N D N D O O O M M M M 100 M M 50 1 ) Biomass (g WW m 0 0 J J J J J J J J J F F F C S S S A A A A A A N D N D N D O O O M M M M M M 0.04 P. flesus -1 C 0.03 ) -2 160 8 month P. flesus 0.02 -2 140 7 Density (Ind m 120 6 0.01 100 5

80 4 g WW m 0 J J J J J J J J F F F S S S A A A A A A N D N D N D O O O M M M M 60 3 M M 40 2 -2 Biomass (g WW m 20 1 ) D 0.005 0 0 P. minutus -1 J J J J J J J J J F F F S S S A A A A A A N D N D N D O O O M M M M M M 0.004

0.003 month

D -2 16 30 0.002 ) P. minutus Density (Ind m -2 14 25 0.001 12

20 g WW m 10 0 J J J J J J J J F F F S S S A A A A A A N D N D N D O O O M M M M 8 15 M M 6 10 4 -2 E 0.0015 2 5 ) P. microps -1 Biomass (g WW m 0 0 0.0012 J J J J J J J J J F F F S S S A A A A A A N D N D N D O O O M M M M M M 0.0009 month

-2 0.0006 E 6 60

) P. microps 0.0003 Density (Ind m -2 5 50

g WW m 0 4 40 J J J J J J J J F F F S S S A A A A A A N D N D N D O O O M M M M M M

3 30 2003 2004 2005 2006 2 20 Fig. 4. Monthly variation of production along the three-year study period for: -2

1 10 ) (A) Dicentrarchus labrax; (B) Solea solea; (C) Platichthys ﬂesus; (D)

Biomass (g WW m 0 0 Pomatoschistus minutus; and (E) Pomatoschistus microps. J J J J J J J J J F F F S S S A A A A A A N D N D N D O O O M M M M M M 2003 2004 2005 2006 Biomass Density with lower biomass (Fig. 3B). In 2006, there was a decrease in density, biomass and production (Figs. 3B and 4B). Platichthys Fig. 3. Monthly variation of mean density and mean biomass along the flesus was the least productive of the nursery species. Its pro- three-year study period for: (A) Dicentrarchus labrax; (B) Solea solea; (C) duction maintained similar values throughout the study period, Platichthys flesus; (D) Pomatoschistus minutus; and (E) Pomatoschistus microps. with exception of May 2004 and from June to December 2005, when production decreased considerably (Fig. 4C), altogether 56 M. Dolbeth et al. / Estuarine, Coastal and Shelf Science 78 (2008) 51e60 with the density and biomass decreases (Fig. 3C). The produc- development in the estuary could be followed, C3 showed a - tion of the resident species was at least three-fold lower than noticeably higher production than C4 (Fig. 5A). The lack of the nursery species. Density attained similar or higher values a significant part of the other cohorts (only the larger individ- than the nursery species, yet the biomass was considerably uals in C2 and only the juveniles in C5) does not enable to lower (Fig. 3D,E). Pomatoschistus minutus showed the highest have a comparable measure of their productive potential and increases of density, biomass and production in 2003/04, de- exportation (Fig. 5A). Yet, the mean monthly production for creasing afterwards to considerably lower values from 2005 the same selected time period and similar length class interval until the end of the study period (Figs. 3D and 4D). Pomato- was also estimated (Table 2). With this procedure comparisons schistus microps had the highest density, biomass and produc- could be made regarding the production potential of three tion values in 2003 and in the winter of 2004/05 (Figs. 3E and consecutive recruitments, based on the youngest individuals 4E). (Table 2). For D. labrax, there was a clear decrease over the three-year study period, with the highest production obtained 3.3. Recruitment and potential for exportation of nursery for the recruits of 2003, followed by considerably lower fish species production for the recruits of 2004 and 2005 (Table 2). For Platichthys flesus and Solea solea the recruitment For Dicentrarchus labrax recruitment occurred systemati- period was not as constant in time as for Dicentrarchus labrax. cally in June (Fig. 5A). Individuals stayed in the estuary until Solea solea recruitment seemed to occur in January (Fig. 5B). at least 18e19 months (see cohorts C2, C3 and C4), disappear- Yet, in 2006 recruitment was clearly delayed to April (C6), as ing afterwards by the end of JanuaryeFebruary, when individ- extremely small size length classes appeared only in April uals reached 20e25 cm in total length (Fig. 5A). After this (Fig. 5B). Similarly to the other species, individuals of S. solea period, only few larger individuals were found (between 2 disappeared the estuary around by November/December, no and 3 years old, Fig. 5A). Comparing the mean annual produc- individuals were caught with more 25 cm and approximately tion of cohorts C3 and C4, the only ones whose complete 20 months (Fig. 5B). Older individuals returned to the estuary occasionally (C3 and C4, Fig. 5B). Only C4 could be followed throughout its complete estuarine lifespan (Fig. 5B). The A 35 D. labrax production of S. solea recruits from 2003 and 2004 was similar 30 2+ 2y 2+ and decreased considerably with the recruits of 2005 (Table 2). C1 -2 -1 25 2y 0.29gm y 1+ Regarding Platichthys flesus, recruitment seemed to occur 1+ 20 1y 1y 0.07gm-2y-1 in April (clear in 2004 and 2006). With the present data, this 15 1y April recruitment was not evident in 2003 and 2005, as in C2 10 0y 2003 there was no data before June, and in 2005 the new 0y 0y 5 cohort only appeared in July (C3 and C5 respectively, Mean length (cm) C3 C4 C5 C6 0 Fig. 5C). It is difficult to ascertain if the recruitment of April J J J J J J J J J F F F S S S A A A A A A N D N D N D O O O M M M M M M was delayed to June/July or if no juveniles were caught in April/May 2005. However, individuals caught in July 2003 B 40 S. solea 2+ and 2005 were larger than 6 cm, which was the same length 35 2y C1 2y 2+ of the July 2004 individuals (Fig. 5C). Platichthys flesus indi- 30 2y 25 viduals stayed at least two years in the estuary, migrating C2 0.17gm-2y-1 20 1y 1y around AprileMay (Fig. 5C). Larger individuals showed 15 1y only occasional occurrence and completely disappeared before 10 0+ 0y 0y 5 0y Mean length (cm) C3 C4 C5 C6 0 Table 2 J J J J J J J J J F F F S S S A A A A A A N D N D N D O O O M M M M M M Monthly production of the selected lengths and time interval for the three consecutive cohorts of the nursery species (Dicentrarchus labrax, Platichthys C 35 P. flesus flesus and Solea solea) 2+ 30 2y Cohort Recruitment Length Time interval Production 0.033gm-2y-1 25 interval (months) per month 2 C2 2y (cm) (g WW m 20 1y month1) 15 1y D. labrax 3 2003 4e12 10 0.031 10 0y 4 2004 4e14 10 0.007 5 0y Mean length (cm) C3 C4 C5 C6 5 2005 5e14 10 0.009 0 S. solea 3 2003 7e20 10 0.015 J J J J J J J J J F F F S S S A A A A A A N D N D N D O O O M M M M M M 4 2004 6e23 10 0.014 2003 2004 2005 2006 5 2005 6e19 10 0.006 P. flesus 3 2003 8e14 9 0.006 Fig. 5. Linear growth of the nursery species (Dicentrarchus labrax, Solea solea 4 2004 7e14 9 0.005 and Platichthys flesus) standard deviation, with indication of production of the 5 2005 7e14 9 0.001 seawards migrating individuals for a selected length interval and time period. M. Dolbeth et al. / Estuarine, Coastal and Shelf Science 78 (2008) 51e60 57 achieving three years (Fig. 5B,C). Only C4 could be followed throughout its complete estuarine lifespan (Fig. 5B). Similarly to Solea solea, the production of P. flesus recruits from 2003 and 2004 was similar, but it decreased considerably with the recruits of 2005 (Table 2). Comparing the production assessed for the partial cohorts of all species, the highest values were observed for Dicentrarchus labrax recruits of 2003, followed the recruits of Solea solea of Elliott and Taylor, 1989 Pombo et al., 2007 2003 and 2004 (Table 2). The lowest partial cohort production Reference

was obtained for Platichthys ﬂesus recruits (Table 2). 1 y 2 4. Discussion 0.020 (0.068) Present study 0.107 (0.119) e 4.1. Fish production general considerations e * Pihl and Rosenberg, 1982 * Hostens and Hamerlynck, 1994 2.63 2.39 pecies contributing for each group e Fish populations are very dynamic due to ﬂuctuating levels e of recruitment and migration (Costa et al., 2002; Cowley and 0.40 e 0.39 Resident species production g WW m

Whitﬁeld, 2002; Pombo et al., 2007), which bears problems 1 y

when trying to estimate their production. In estuaries, several 2 fishes have only an occasional occurrence, while others mi- grate according to age and hydrological environment (Elliott 0.596 (0.66) 0.160 (0.178) 0.75 (2.50) 0.005 (0.015) e and Dewailly, 1995; Costa et al., 2002), conditioning a correct * e assessment of their population dynamics. Accurate estimates * 1.27 1.88 29.40 e e of fish production are provided with both a short time interval e relative to the population dynamics of the fish and with a large production g WW m 3 sps 2 sps 1 sp 2 sps 3 sps 1sp 2 sps 4 sps 4 sps population size (Elliott, 2002). Therefore, the present study dealt only with the production estimation for the most abun- ); between brackets production after correction for the catch efficiency of the sampling gear. dant fish species of the Mondego estuary. These comprised more than 75% of the whole fish community density for the 2.5 2.01 ¼ Brey, 2001 studied years (Martinho et al., 2007b) and about 56% of the B / community biomass (unpublished data). Estimates were repre- P sentative of the nursery species production (100% of density and biomass), and of the resident species production (88% of density and 63% of the biomass) potential within the Instantaneous growth 0.015 (0.02) estuary. Negative production values were not accounted for the production estimates. In fish populations, these negative productions have been associated to possible migration and/or size selective mortality and have been accounted for the production estimates (Costa et al., 2002; Pombo et al., 2007). The studied species are supposed to spend their life cycle (resident) or their beach-seine net

early life stages (nursery) in the estuary (Elliott and Dewailly, were converted to WW (WW-AFDW: 0.251, 1979 Drop trap1985 Beam trawl Cohort2000 Increment summation ‘‘Chincha’’, traditional 1.16 Instantaneous growth2006 Beam trawl 1.15 Cohort Increment summation 0.39 (1.33) e 1995), therefore the negative values were not considered for e e e e the annual production estimates evaluation, as these could 1978 1982 1987/881999 Beam trawl2003 Empirical: 2 lead to an underestimation of the estuarine production. ADFW 2 2 2 2 e 4.2. Resident and nursery species production

In general, the production of the resident and the marine juvenile species of the Mondego estuary seemed lower when compared to other estuarine systems, even after correcting the production estimates for the catch efﬁciency of the sampling gear (beam trawl) (Table 3). As a result, the expectation that production would increase with decreasing latitudes (Cowley and Whitﬁeld, 2002) did not occur, similarly to the

findings of Pombo et al. (2007), though this relationship Original units in ash free dry weight * Table 3 Comparison of production estimates in European estuaries for resident and nursery species (flatfishes and seabass), with indication of the number of s Location Area Study period Sampling gear Production estimation method Nursery species Forth estuary, Scotland 84 km Oosterschelde estuary, Netherlands 351 km Mondego estuary, Portugal 3.4 km Ria de Aveiro, Portugal 47 km occurred with the macrozoobenthic intertidal community Skagerrak (Gullmarsvik), Sweden 15 km 58 M. Dolbeth et al. / Estuarine, Coastal and Shelf Science 78 (2008) 51e60 production (Dolbeth et al., 2007b). There are several possible the study period and similar values to other systems else- sources of error when assessing the fish production (more where (0.02 for the Irish Sea, Costa et al., 2002, and detailed information in Costa et al., 2002 and Cowley and 0.24 g WW m2 y1 for Osterschelde estuary, Hostens and Whitfield, 2002), which turns difficult to compare with other Hamerlynck, 1994). Pomatoschistus minutus showed a consid- estimates elsewhere. Nevertheless, hypotheses related with erable decrease in production in the drought year of 2005 con- environmental pressures (discussed later in text) within the es- trarily to P. microps, which is more tolerant to higher 1 tuary or its relatively small area (at least less than ⁄4 area than temperatures (Fonds and Buurt, 1974). More details and com- the other studied ecosystems, Table 3) may be suggested. It is parisons of both Pomatoschistus spp. productions can be found also possible that an important part of the fish production was in Dolbeth et al. (2007a). not accounted, as the fish inhabiting the seagrass and saltmarsh areas of the Mondego estuary were not correctly assessed. 4.3. Implications of anthropogenic and natural impacts These are known as important nursery areas, providing both food and shelter for several small fishes (Beck et al., 2001; Important anthropogenic impacts have been occurring in Costa et al., 2001; Cabral et al., 2007), and where fish produc- the Mondego estuary that, to certain extent, might have com- tion can be considerably higher compared to unvegetated areas promised the fish production. Among anthropogenic impacts (Edgar and Shaw, 1995). Moreover, the relative low density affecting the fish community, bank reclamation (due to port and biomass of the marine species, hence production, may activities and agriculture), fishing and eutrophication, with be attributed to the small area compared to other systems, consequent reduction of the seagrass beds (more details in and small opening of the Mondego estuary, which may limit Cardoso et al., 2005; Dolbeth et al., 2007b), were considered the entrance of marine species (Martinho et al., 2007b). How- as major impact sources (Martinho et al., 2007b; Vasconcelos ever, in some occasions, the nursery species production of the et al., 2007). Although there are no fish production estimates Mondego overcame the estimates from other estuaries and from the past, it is quite plausible that the production might coastal lagoons (Table 3). have decreased, both due to a decrease of alternative habitats For the Mondego estuary, the annual production of the (Leit~ao et al., 2007; Martinho et al., 2007a; Vasconcelos et al., nursery species was higher than the production of the resident 2007) and due to the overall decrease in the macrobenthic ones, contrarily to Pombo et al. (2007), where Atherina boyeri, production (Dolbeth et al., 2007b). The decrease in the macro- a pelagic resident species (not easily caught by the beam trawl benthic production means a decrease in food availability, as used in the present study), had a high production in the estu- the studied species feed intensively on the macrobenthos ary. In general, the resident species attained higher densities (Leit~ao et al., 2006; Martinho et al., in press). Also, trends (especially Pomatoschistus microps in 2004e2006) but these of the fish community over the last two decades showed lower coupled with considerably low biomasses, resulted in lower fish diversity at the present time (Leit~ao et al., 2007). productions. Among the nursery species, Dicentrarchus labrax Estuaries are exposed to severe of anthropogenic and inher- was the most productive. Similar production values were ent natural stress, being difficult to distinguish between the obtained in the Ria the Aveiro, also in Portugal (0.02e two sources of impacts (Elliott and Quintino, 2007). The fish 0.66 g WW m2 y1, Pombo et al., 2007), yet few data exists community composition, as well as the population dynamics on the sea bass production in natural conditions elsewhere for of single species, seems to be strongly affected by density in- comparative purposes (Costa et al., 2002). The production dependent factors, such as temperature, salinity, wind regime, seemed to decrease after the migration period, hypothesized tides (among others) in several estuarine systems (Marshall to occur between January/February, which agrees with down- and Elliott, 1998; Powers et al., 2000; Costa et al., 2002; stream dispersion of the older individuals occurring in the Maes et al., 2004; Akin et al., 2005). Regarding climate winter and early spring (Leit~ao et al., 2007; Martinho et al., variability impacts on the Mondego estuary within the study 2007a). For Platichthys flesus, production decreases after the period, the gradual occurrence of a drought (starting by a nor- migration period was not so clear. Annual production was mal hydrological year in 2003 and attaining a severe drought lower than the one observed in the Forth estuary (around in 2005), high water temperatures and low freshwater dis- 1.3 g WW m2 y1, Elliott and Taylor, 1989) where this charges seemed the most relevant episodes. Accordingly, the species behaves as resident (Elliott and Dewailly, 1995), but production showed a clear decrease during the dry year of similar with other systems elsewhere (0.07 for the Elbe and 2005, with the highest decreases observed for Dicentrarchus 0.16 g WW m2 y1 for the Oosterschelde estuaries, Costa labrax, Platichthys flesus and Pomatoschistus minutus.Itis et al., 2002). Although it was not concluded a preference of difficult to ascertain the main factors for this decrease (in this species for colder waters (within a range of 11e26 C), agreement to the ‘‘Estuarine Quality Paradox’’, Elliott and the north and central coast of Portugal (i.e., Mondego estuary) Quintino, 2007), yet experimental studies have revealed the appears to be the southern limit for the distribution of P. flesus limiting effect of high temperatures and salinity variations (Cabral et al., 2007). Also, the decrease in more southern areas on eggs and larval development of P. minutus and Pomato- (e.g. Tagus estuary) has been associated to increases in water schistus microps (Fonds and Buurt, 1974) and of P. flesus (Ca- temperature (Cabral et al., 2001), which also occurred in the bral et al., 2007). Solea solea seems more tolerant to variations Mondego estuary and could explain the lower productions ob- in temperature and salinity (Fonds, 1975). Some studies have tained. Solea solea maintained a similar production throughout also showed a positive influence of moderate river discharges M. Dolbeth et al. / Estuarine, Coastal and Shelf Science 78 (2008) 51e60 59 for an overall increase in primary production of estuarine sys- 2005; Gillanders, 2005). Nevertheless, at least part of the tems (Houde and Rutherford, 1993; Costa et al., 2002, 2007; cohort from consecutive recruitments, occurring in different Vinagre et al., 2007), with consequent impacts on the produc- hydrological years (i.e., with gradual drought effect) could tion of the other trophic levels. Additionally, river drainage has be assessed and their consequent potential production for been positively associated with marine juvenile densities, due exportation evaluated and compared. For Platichthys flesus to the existence of chemical cues used by their larvae for and Solea solea the lowest production was observed when movement orientation into the estuary (Costa et al., 2007; Vi- the recruitment occurred in 2005, the extreme dry year. For nagre et al., 2007). Drought and the consequent decrease in Dicentrarchus labrax a clear reduction in production was river discharge will lower both the primary production and also observed in 2005, but the lowest value was obtained in the chemical cues reaching coastal waters, less detectable by 2004, also a dry year. Such reduction in production (and larvae. These relationships between fish abundance and fresh- potential reduction of emigrating fish) could influence the bio- water flow may be quite different according to species (Costa diversity and stability of the neighbouring inshore coastal or et al., 2007), and several studies have showed an increase in shelf ecosystems (Cowley and Whitfield, 2002). Ultimately, the fish community density in dry years (Costa et al., 2007). this could affect the economy, due to the high commercial Yet, others showed that the recruitment of the marine species value of the studied species. could be reduced (Costa et al., 2002), as well as the overall density of the resident species (Martinho et al., 2007b). Alto- gether, these studies highlight the hypothesis that salinity, tem- Acknowledgements perature and river discharge variations may be major driving forces acting in the recruitment success and population devel- The authors are indebted to Daniel Crespo, Heliana Teix- opment of the studied species, due to high natural mortality. eira, Jo~ao Miguel Neto, Ricardo Leit~ao and Tiago Verdelhos This change in the environmental conditions might have in- who helped in field work. This work was supported by the creased the predation pressure by piscivorous fishes (mostly FCT (Portuguese Foundation for Science and Technology) marine adventitious species) whose abundance increased in through a PhD grant attributed to M. Dolbeth (SFRH/BD/ the estuary (Martinho et al., 2007b), or induced seawards mi- 14112/2003). gration, as also suggested by Dolbeth et al. (2007a) for the resident species. Additionally, for the marine spawning fishes, it is also important to consider other unmeasured aspects that References might have influenced the recruitment, such as reproductive Able, K.W., 2005. A re-examination of fish estuarine dependence: evidence for success on continental shelf related with the oceanographic connectivity between estuarine and ocean habitats. Estuarine, Coastal and conditions (Vinagre et al., 2007). Shelf Science 64, 5e17. Ultimately, the decrease in the fish production may have Akin, S., Buhan, E., Winemiller, K.O., Yilmaz, H., 2005. Fish assemblage important consequences for the adult stocks of the marine spe- structure of Koycegiz Lagoon Estuary, Turkey: spatial and temporal cies (see below) and for the estuarine food web, as the resident distribution patterns in relation to environmental variation. Estuarine, Coastal and Shelf Science 64, 671e684. species are dominant prey of several other fishes (Dolbeth Beck, M.W., Heck, K.L., Able Jr., K.W., Childers, D.L., Eggleston, D.B., et al., 2007a). Gillanders, B.M., Halpern, B., Hays, C.G., Hoshino, K., Minello, T.J., Orth, R.J., Sheridan, P.F., Weinstein, M.P., 2001. The identification, 4.4. Exportation of commercially important fish species conservation, and management of estuarine and marine nurseries for fish and invertebrates. Bioscience 51, 633e641. Brey, T., 2001. Population dynamics in benthic invertebrates. A virtual Estuaries are crucial for the overall development of several handbook. Version 01.2. Alfred Wegener Institute for Polar and Marine fish populations and what happens in the estuarine system may Research, Germany. http://www.awi-bremerhaven.de/Benthic/Ecosystem/ compromise the coastal stocks and ultimately the fisheries, FoodWeb/Handbook/main.html. with important socio-economic impacts (Houde and Ruther- Cabral, H.N., Costa, M.J., Salgado, J.P., 2001. Does the Tagus fish community e ford, 1993). Several marine spawning fishes have an estuarine reflect environmental changes? Climate Research 18, 119 126. Cabral, N.H., Vasconcelos, R.P., Vinagre, C., França, S., Fonseca, V., Maia, A., residence phase during the early life cycle and then an emigra- Reis-Santos, P., Lopes, M., Ruano, M., Campos, J., Freitas, V., Santos, P., tion back to the coastal areas (Cabral et al., 2007; Martinho Costa, M.J., 2007. Relative importance of estuarine flatfish nurseries along et al., 2007a). This emigration will transfer large amounts of the Portuguese coast. Journal of Sea Research 57, 209e217. energy, which was accumulated in the estuary (Cowley and Cardoso, P.G., Brand~ao, A., Pardal, M.A., Raffaelli, D., Marques, J.C., 2005. Whitfield, 2002; Gillanders et al., 2003). In fact, in several Resilience of Hydrobia ulvae populations to anthropogenic and natural disturbances. Marine Ecology Progress Series 289, 191e199. locations, a fraction higher than 50% of the fisheries harvests Costa, M.J., Catarino, F., Bettencourt, A., 2001. The role of salt marshes in the is estuarine or estuarine-dependent in at least some life stages Mira estuary (Portugal). Wetlands Ecology and Management 9, 121e134. (Houde and Rutherford, 1993; Able, 2005). In the present Costa, M.J., Cabral, H.N., Drake, P., Economou, A.N., Fernandez-Delgado, C., study, a direct measurement and comparison of each recruit- Gordo, L., Marchand, J., Thiel, R., 2002. Recruitment and production of ment production contribution to exportation was not possible, commercial species in estuaries. In: Elliot, M., Hemingway, K. (Eds.), Fishes in Estuaries. Blackwell Science, United Kingdom, pp. 54e123. as not all the cohorts could be followed completely. It is also Costa, M.J., Vasconcelos, R., Costa, J.L., Cabral, H.N., 2007. River flow difficult to evaluate the actual connectivity of this estuarine influence on the fish community of the Tagus estuary (Portugal). Hydrobio- production to the coastal area (Gillanders et al., 2003; Able, logia 587, 113e123. 60 M. Dolbeth et al. / Estuarine, Coastal and Shelf Science 78 (2008) 51e60

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